Directory UMM :Data Elmu:jurnal:T:Tree Physiology:Vol16.1996:
Tree Physiology 16, 583--589
© 1996 Heron Publishing----Victoria, Canada
Effects of soil and stem base heating on survival, resprouting and gas
exchange of Acer and Quercus seedlings
JULIE A. HUDDLE1,2 and STEPHEN G. PALLARDY1
1
School of Natural Resources, University of Missouri, Columbia, MO 65211, USA
2
Present address: Department of Rangeland Ecology and Management, Texas A&M University, College Stat
ion, TX 77843, USA
Received June 6, 1995
Summary Acer rubrum L., A. saccharum Marsh., Quercus
alba L. and Q. rubra L. seedlings subjected to soil and stem
base heat treatments showed rapid declines in rates of transpiration and photosynthesis. Reductions in photosynthetic rate
were partly attributable to mesophyll inhibition. Quercus seedlings were less able to maintain transpiration and photosynthesis after heat treatment than Acer seedlings. Declines in rates
of transpiration and photosynthesis of Quercus seedlings were
observed 1 h after heat treatment and became more pronounced
over time. In contrast, rates of transpiration and photosynthesis
of Acer seedlings initially declined in response to heat treatment, partially recovered after one or two days, but then
declined again six to eight days after the heat treatment. Observed changes in leaf water potential after heating were small,
suggesting that hydraulic factors were not the primary signal
eliciting the gas exchange response to soil and stem heating.
Ultimately, the heat treatments caused stem die-back of
most seedlings. For all species, seedlings that resprouted had a
greater chance of surviving heat stress than seedlings that did
not resprout. Despite the rapid loss of photosynthetic capacity
in response to heat treatment in Quercus seedlings, survival
was higher in Quercus seedlings than in Acer seedlings, and
was associated with a greater capacity for resprouting. We
suggest that the reduced allocation of resources toward recovery of photosynthesis in existing Quercus stems after heat
stress is a physiological mechanism that facilitates resprouting
and hence survival of Quercus seedlings after fire.
maple and sugar maple (Acer rubrum L., A. saccharum
Marsh.) (Carvell and Tryon 1951, Lorimer 1989, Abrams and
Downs 1990, Nowacki et al. 1990, Johnson 1992). A better
understanding of the physiological responses of species to fire
would allow fire prescriptions (e.g., season, weather conditions during burning) to be adjusted to favor establishment of
desired species.
Reich et al. (1990) found that photosynthesis increased
several weeks after burning in surviving black cherry (Prunus
serotina Ehrh.), northern pin oak (Quercus ellipsoidalis E.J.
Hill) and blackberry (Rubus allegheniensis Porter) plants, but
not in A. rubrum. Long-term increases in insolation and available nutrients after fire may alter physiological processes such
as photosynthesis (Ahlgren and Ahlgren 1960, Viro 1974,
Reich et al. 1990) that may be associated with mortality or
survival soon after fire. In one of the few studies on short-term
physiological responses of species to fire, Van Sambeek and
Pickard (1976a, 1976b) showed that scorching of leaves of
herbaceous species by fire was followed by rapid changes in
gas exchange of unheated leaves.
In an attempt to elucidate the mechanisms underlying the
physiological responses to fire of species that are differentially
tolerant of fire in natural ecosystems, we studied the effects on
gas exchange and survival of briefly heating surface roots and
stem bases of seedlings of red maple, sugar maple, white oak
(Quercus alba L.) and northern red oak (Quercus rubra L.).
Keywords: Acer saccharum, Acer rubrum, fire, photosynthesis,
Quercus alba, Quercus rubra, resprouting, survival, thermotolerance, transpiration.
Materials and methods
Introduction
In forest ecosystems, mortality caused by fire is selective
against many invading mesic species, suggesting that fire
might be used as a tool to control species composition and
diversity (Curtis 1959, Crow 1988). Fire is an important factor
in the establishment and maintenance of many oak-dominated
forests in the eastern USA, forests that otherwise would tend
to be replaced by more mesic, fire-sensitive species such as red
Seedling culture
Seeds of Q. alba, Q. rubra, A. rubrum, and A. saccharum were
collected from the Columbia area. Acorns and sugar maple
seed were collected in the fall of 1992, and red maple seed was
collected in the spring of 1991. Purchased red maple seed
(F.W. Schumacher Co., Inc., Sandwich, MA) was used in the
spring of 1993. Seeds were stratified and germinated according
to standard protocols (USDA Forest Service 1974).
Germinants were planted in a greenhouse in cylindrical
5.6-liter pots (15.3 cm diameter, 30.5 cm tall) filled with a
1/2/1 (v/v) mixture of peat moss, sand and silt loam. After
584
HUDDLE AND PALLARDY
planting, 30 ml of slow-release 14,14,14 N,P,K fertilizer (Osmocote, San Milpitas, CA) was placed on the soil surface and
30 ml of vermiculite layered on top to retard evaporation. Pots
were watered once a week, and fertilized weekly with modified Hoagland’s solution (Johnson et al. 1957). The temperature of the greenhouse ranged between 10 and 43 °C during the
study. Sunlight supplemented with sodium vapor lamps kept
midday irradiances at seedling tops at approximately 1000
µmol m −2 s −1 photosynthetic photon flux density (PPFD).
Growth chamber conditions and heating treatments
Before heat treatment, seedlings were moved from the greenhouse to a growth chamber and allowed to acclimate for at least
three days. The growth chamber provided a temperature of
25 °C and a 14-h photoperiod (400 µmol m −2 s −1 PPFD at the
top of the seedlings). Mean age at treatment ranged from 118
days for A. saccharum seedlings to 133 days for Q. alba
seedlings, with no significant differences among species (P ≤
0.05).
To simulate the heat of a passing ground fire, one of two
aluminum block heaters, one with a plate containing a 1.0 cm
slot and a 1.25 cm diameter hole, the other with a plate
containing a 2.0 cm slot and a 4.0 cm diameter hole, was used
(Figure 1). The block heater with the larger slot width and
central ring diameter was fabricated to reduce the number of
seedlings for which data had to be discarded because of inadvertent direct contact between the plate and stem. Two ceramic
cartridge heaters (Type 500B, Standard Electric Products Co.,
Dayton, OH) placed in holes drilled in the block provided
heating. Before the heat treatment was begun, the top of the
seedling was enclosed in a 2.54-liter water-cooled cuvette with
PPFD maintained at 2000 µmol m −2 s −1 with a multi-vapor
lamp (General Electric, Hendersonville, NC). Seedlings were
not removed from the cuvette until at least 60 min after applying heat.
After gas exchange had equilibrated, power (80 V, 7.5 amps)
was applied to the heaters and the heated block was then placed
on the soil. Mean duration of heat treatment ranged from 9.7
to 10.5 min with no significant differences among species.
Among species, mean maximum stem base temperature during
treatments ranged from 76.6 to 85.8 °C, with no significant
differences among species. Among individual seedlings, Tstem
ranged from 33 to 180 °C, and appeared to be dependent on
small differences in placement of the plate. Although there was
substantial variation in stem base temperature, it was not
unlike what might be expected in a natural surface fire event.
Nearly every heat treatment elicited a gas exchange response,
and variation in stem base temperature did not obscure species
differences in survival, resprouting or gas exchange responses.
Complete sets of gas exchange data were available for between
15 and 20 seedlings per species.
Temperatures at the base of the seedling stem and at three
soil depths in the pot were monitored throughout the gas
exchange measurements with copper-constantan thermocouples (Figure 2). Holes drilled on one side of the pot allowed
thermocouples to be inserted at several soil depths (Figure 1).
Leaf temperature and air temperature inside the cuvette were
also monitored.
Gas exchange measurements
Photosynthesis at 33--35 Pa ambient CO2 partial pressure and
transpiration were monitored with an open gas exchange system described by Ni and Pallardy (1991). Instrument outputs
were acquired every 10 s by a computerized data logger.
Photosynthesis (A, µmol m −2 s −1), transpiration (E, mmol m −2
s −1) and internal partial pressure of CO2 (Ci, Pa) were com-
Figure 1. Three-dimensional view of a heating plate and seedling.
Wires indicate the point at which two ceramic cartridge heaters were
inserted in the heating plate. Note sections of each pot were cut away
to facilitate placement of the heating plate and holes were drilled in the
side of each pot to provide for placement of thermocouples at several
soil depths. The top of the seedling was enclosed in a gas exchange
cuvette during the heating treatment.
Figure 2. Examples of temperatures during heating treatments. Symbols designate where temperatures were measured: (for Q. rubra 1) m
at stem base, h at 0.5 cm soil depth, , at 2.0 cm soil depth, n at
4.5 cm soil depth; (for A. saccharum 5) m at stem base, h at soil
surface, , at 1.5 cm soil depth, n at 4.0 cm soil depth.
STEM AND SOIL HEATING AND SEEDLING SURVIVAL
puted using equations of von Caemmerer and Farquhar (1981).
Photosynthesis and E of the heat-treated seedlings were monitored for several days after heating during which time seedlings were watered frequently. Because the pretreatment gas
exchange rates varied among seedlings, comparisons were
based on ratios of post-treatment to pretreatment values.
Water potential measurements
During the gas exchange measurements, the leaf water potential (Ψleaf ) of between six and eleven seedlings per species was
measured every 4 to 6 min with two leaf hygrometers (Model
L-51, Wescor, INC., Logan, UT) attached to leaves inside the
cuvette. The hygrometers were calibrated with KCl solutions
of known molality as described by Pallardy et al. (1991).
Assessment of survival and resprouting
Two weeks after heating, seedlings were moved from the
growth chamber back to the greenhouse. Watering and fertilization were conducted every week as described previously.
Resprouting and survival of all heat-treated seedlings (22--25
seedlings per species) were monitored for 12 weeks in the
greenhouse.
Statistical analysis
Chi-square tests were conducted to detect statistically significant differences among species in survival and resprouting
(Snedecor and Cochran, 1980). A chi-square test was also used
to detect statistically significant differences in survival between resprouting and non-resprouting seedlings.
Although soil temperatures increased in response to the heat
treatment, it was not possible to compare results across seedlings because of variations associated with measurement depth
and technical difficulties. Therefore, the maximum temperature measured at the base of the stem (Tstem ) was used as a
measure of temperature experienced by seedlings.
The statistical tests used to determine the significance of gas
exchange responses after heating were based on 95% tolerance
limits calculated for 1-min averages of gas exchange parameters (A, E, and Ci) measured before treatments were applied
(Hald, 1952). Similarly, the 95% tolerance limits of gas exchange responses 1 h after heat treatment were calculated from
585
1-min averages between 55 and 65 min after the heat treatment
was applied for each seedling. Responses 1 h after heating
were scored as 0, if the tolerance limits overlapped, or as 1 if
the tolerance limits did not overlap.
Short-term response scores (RS = 0 or 1) were then averaged
for each combination of species and three ranges of Tstem
(45--75, 75--105 and 105--135 °C). These averages were
arcsine transformed to normalize error as described by Box
and Cox (1964). The General Linear Models procedure of the
SAS version 6.08 software prgram (SAS Institute, Cary, NC)
was used to conduct analysis of variance (ANOVA) and to
calculate least square means with species and Tstem as treatment effects.
To analyze the magnitude of the short-term gas exchange
response, percent change in each parameter was calculated for
each seedling as follows:
%∆G s =
G 1 − G0
100 ,
G0
where %∆Gs is the short-term percent change in a gas exchange parameter, G1 is the mean of the parameter 1 h after
treatment and G0 is the mean of the parameter before heat was
applied. Percent changes in gas exchange were then arcsine
transformed to normalize error and analyzed by ANOVA with
species, response score 1 h after treatment (RS1 h) and the
interaction between species and response score as treatment
effects. Calculated least square means were subjected to the
t-test to determine whether they were significantly different
from zero.
Long-term changes in gas exchange parameters (%∆Gl)
were calculated and analyzed as describd for the short-term
changes. Data were pooled in two categories (1--2 days after
treatment, Dj = 1; and 6--8 days after treatment, Dj = 7) and
compared with pretreatment values:
%∆G 1 =
G j − G0
100 ,
G0
where Gj is the mean of the gas exchange parameter on day j
(Dj) after treatment and G0 is the mean of the gas exchange
Table 1. Survival and resprouting frequency of each species. Percentages in a row with different letters are significantly different (P ≤ 0.05).
Non-surviving seedlings
Non-resprouting
Resprouting
Total
Surviving seedlings
Non-resprouting
Resprouting
Total
% Survival
% Resprouting
Acer
rubrum
Acer
saccharum
Quercus
alba
18
0
18
21
0
21
10
3
13
2
1
3
51
4
55
1
3
4
1
0
1
1
11
12
4
18
19
7
32
39
4.5 c
0.0 b
48.0 b
56.0 a
88.0 a
76.0 a
41.5
38.3
18.2 c
13.6 b
Quercus
rubra
Total
586
HUDDLE AND PALLARDY
parameter before treatment. These percentages were transformed and analyzed by ANOVA with species, Dj and the
interaction between species and Dj as treatment effects. Each
least square mean was tested to detect whether it was significantly different from zero and back transformed to a percentage.
Results
Survival and resprouting
Survival among resprouting seedlings was significantly
greater (P ≤ 0.05) than among non-resprouting seedlings (88.9
versus 12.1%). Both Quercus species had significantly greater
survival and resprouting rates than either Acer species (Table 1), although only the difference in survival was statistically
significant. For all species, mean Tstem did not differ (P ≤ 0.05)
between non-surviving, non-resprouting seedlings (82.4 °C)
and surviving, resprouting seedlings (87.7 °C).
heat treatment than Acer seedlings. For all species, the shortterm percent change in photosynthetic rate, %∆As, declined
significantly only for seedlings with an RS = 1 (Table 3). Of
seedlings with an RS = 1, the relative reduction in A of
A. rubrum seedlings was significantly less than that of either
of the Quercus species. Internal CO2 partial pressure usually
increased, at least transiently, after heat application, except in
a few A. rubrum seedlings. For all seedlings, average %∆Ci,s
1 h after heat treatment was 1.4%. Mean %∆Ci,s increased for
all combinations of species and response scores after heat
treatment (Table 3).
Because the standard error of E increased between the pre-
Short-term gas exchange dynamics
At least 60% of all seedlings showed significant short-term
responses (i.e., RS = 1) in Ci, E and A to the heat treatment
(Table 2). Although the fraction of seedlings showing significant changes in Ci and E following heating increased with
increasing Tstem , the trend was not significant (P ≤ 0.15). In
contrast, the fraction of seedlings showing significant change
in A following heat treatment increased significantly (P ≤ 0.01)
with increasing Tstem (Table 2).
Heat-induced declines in A and E were usually apparent
within 1 h of heat treatment (cf. Figures 3 and 4). Averaged
across all species, seedlings showed a mean decline of 23.7%
in A 1 h after the heat treatment. Gas exchange of seedlings of
both Quercus species generally showed a greater response to
Table 2. Mean percent of seedlings showing significant responses (i.e.,
a response score of 1) in Ci, E and A by species and Tstem . Means by
species within a column with different lower case letters are significantly different (P ≤ 0.05); means by Tstem within a column with
different upper case letters are significantly different (P ≤ 0.05). All
means differed significantly from zero (P ≤ 0.05). P-values of models
used to calculate means given on the right.
Species
Acer rubrum
Acer saccharum
Quercus alba
Quercus rubra
Ci
E
A
67.4 a
61.2 a
86.3 a
64.2 a
78.7 ab
64.2 b
95.8 a
64.2 b
83.7 ab
72.3 b
95.3 a
82.1 ab
56.7 A
73.0 A
89.5 A
62.2 A
86.6 A
82.0 A
45.2 C
86.6 B
100.0 A
0.20
0.15
0.06
0.12
0.12
Q. alba
> A. rubrum ≈ A. saccharum. Seedlings of both Quercus
588
HUDDLE AND PALLARDY
Table 4. Mean long-term percent changes in Ci, E, and A from pretreatment values between one and two days after treatment (D1) and between six
and eight days after treatment (D7). For each species, means with different lower case letters are significantly different (P ≤ 0.05); for each day,
means with different upper case letters are significantly different (P ≤ 0.05). Means significantly different from zero (P ≤ 0.05) are designated with
asterisks.
Parameter
Day
A. rubrum
A. saccharum
%∆Ci,l
D1
D7
19.5 *a
9.6 *c
1.2 *f
4.5 *e
%∆El
D1
D7
17.7 *a
−32.7 *d
−4.5 b
−18.0 *c
%∆Al
D1
D7
23.7 *a
−34.3 *c
8.9 *b
8.9 *b
species showed significantly greater resprouting rates after
heating than did seedlings of either Acer species, suggesting
that the capacity of Quercus species to resprout after exposure
to lethal stem temperatures enables them to survive fire better
than Acer species (Huddle 1995).
Decreases in E and A and slight increases in Ci were observed after soil and stem base heating was applied, indicating
that changes in leaf gas exchange can occur in response to
application of heat to tissues remote from the leaf (Sinyukhin
and Gorchakov 1966, Van Sambeek and Pickard 1976b). Hydraulic signals may induce physiological responses in tissues
not directly exposed to a variety of stresses, including heat
(Malone 1993, Malone et al. 1994). One type of hydraulic
signal that might be associated with thermal responses is a
change in Ψ. If a hydraulic pulse associated with heating
lowered Ψ of cells surrounding guard cells, the latter may lose
water through passive water movement, resulting in stomatal
closure (Malone 1993). Changes in Ψleaf observed in the present study do not support this hypothesis. The decreases in
water potential never exceeded −0.5 MPa and were usually
smaller, and Ψleaf values never declined to the range over which
stomatal closure might be expected (Bahari et al. 1985, Ni and
Pallardy 1991, 1992). Because Ψleaf remained relatively high
after heating and did not drop more rapidly than E or A, we
conclude that changes in Ψ were not associated with the
heat-induced reductions in A.
An alternative hypothesis is that the declines in E following
heat application are the result of a series of events triggered by
propagation of action potentials that changes guard cell turgor
and causes stomatal closure (Davies 1987, Davies et al. 1991).
Studies with herbaceous plants have shown that if a stimulus
such as heat, cutting or a series of electrical pulses is sufficient
to cause a measurable action potential, a change in gas exchange follows (Gunar and Sinyukhin 1963, Sinyukhin and
Gorchakov 1968, Van Sambeek and Pickard 1976b, Dziubiñska et al. 1989).
Besides lowering E, heat treatment reduced A. Because
stomatal closure reduces availability of CO2, Ci should decline
if stomatal closure is largely responsible for reduced A. However, Ci of most seedlings increased after heat treatment, sug-
Q. alba
Q. rubra
3.2* ef
13.4* b
5.0 *e
7.4 *d
7.2 *B
8.7 *A
−18.6* c
−0.8* c
−32.2 *d
−23.2 *c
−9.4 *A
−18.7 *B
−35.3* c
−60.6* e
−48.9 *d
−56.4 *de
−12.9 *A
−35.6 *B
All species
gesting that increased mesophyll resistance was at least partly
responsible for the observed reductions in A.
On the days following heat treatment, seedlings of both
Quercus species underwent a progressive and more substantial
loss in photosynthetic capacity than seedlings of the Acer
species, whereas we had expected that species more capable of
surviving fire (i.e., Quercus) would maintain or regain physiological function more fully after heating than more poorly
adapted species such as Acer. We postulate that the inverse
relationship between photosynthetic capacity and survival following heat treatment is related to the plant’s capacity to
resprout. Our results indicate that the resprouting response,
which was more vigorous in Quercus species than in Acer
species, is an alternate and effective, but resource-intensive,
adaptation to fire. Based on our results and the findings of other
studies, we suggest that Quercus spp. respond to heat injury
by: (1) abandoning heat-injured shoots; (2) promoting rapid
compartmentalization of injured from healthy tissues by the
production of a suberin layer (McDougall 1993); (3) promoting release from hormonal inhibition associated with apical
dominance of living stems (Vogt and Cox, 1970); and (4)
promoting reallocation of resources to the resprouting response.
Physiological and shoot mortality responses to even moderate heating were substantial, and thus many surface fires in
natural forests could be expected to elicit similar responses in
small individuals to those observed in this study. The more
vigorous resprouting capacity of Quercus compared to Acer
seedlings appears to be a key feature of the successful adaptation of Quercus species to fire. This difference could be exploited to promote greater relative abundance of Quercus
regeneration in deciduous forests of eastern North America.
Acknowledgments
Research was supported by the McIntire-Stennis Program. The
authors thank N. Loewenstein and J. Rhoads for greenhouse assistance, John Roberts for technical assistance, and Dr. G. Krause for
suggestions on statistical analysis.
STEM AND SOIL HEATING AND SEEDLING SURVIVAL
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© 1996 Heron Publishing----Victoria, Canada
Effects of soil and stem base heating on survival, resprouting and gas
exchange of Acer and Quercus seedlings
JULIE A. HUDDLE1,2 and STEPHEN G. PALLARDY1
1
School of Natural Resources, University of Missouri, Columbia, MO 65211, USA
2
Present address: Department of Rangeland Ecology and Management, Texas A&M University, College Stat
ion, TX 77843, USA
Received June 6, 1995
Summary Acer rubrum L., A. saccharum Marsh., Quercus
alba L. and Q. rubra L. seedlings subjected to soil and stem
base heat treatments showed rapid declines in rates of transpiration and photosynthesis. Reductions in photosynthetic rate
were partly attributable to mesophyll inhibition. Quercus seedlings were less able to maintain transpiration and photosynthesis after heat treatment than Acer seedlings. Declines in rates
of transpiration and photosynthesis of Quercus seedlings were
observed 1 h after heat treatment and became more pronounced
over time. In contrast, rates of transpiration and photosynthesis
of Acer seedlings initially declined in response to heat treatment, partially recovered after one or two days, but then
declined again six to eight days after the heat treatment. Observed changes in leaf water potential after heating were small,
suggesting that hydraulic factors were not the primary signal
eliciting the gas exchange response to soil and stem heating.
Ultimately, the heat treatments caused stem die-back of
most seedlings. For all species, seedlings that resprouted had a
greater chance of surviving heat stress than seedlings that did
not resprout. Despite the rapid loss of photosynthetic capacity
in response to heat treatment in Quercus seedlings, survival
was higher in Quercus seedlings than in Acer seedlings, and
was associated with a greater capacity for resprouting. We
suggest that the reduced allocation of resources toward recovery of photosynthesis in existing Quercus stems after heat
stress is a physiological mechanism that facilitates resprouting
and hence survival of Quercus seedlings after fire.
maple and sugar maple (Acer rubrum L., A. saccharum
Marsh.) (Carvell and Tryon 1951, Lorimer 1989, Abrams and
Downs 1990, Nowacki et al. 1990, Johnson 1992). A better
understanding of the physiological responses of species to fire
would allow fire prescriptions (e.g., season, weather conditions during burning) to be adjusted to favor establishment of
desired species.
Reich et al. (1990) found that photosynthesis increased
several weeks after burning in surviving black cherry (Prunus
serotina Ehrh.), northern pin oak (Quercus ellipsoidalis E.J.
Hill) and blackberry (Rubus allegheniensis Porter) plants, but
not in A. rubrum. Long-term increases in insolation and available nutrients after fire may alter physiological processes such
as photosynthesis (Ahlgren and Ahlgren 1960, Viro 1974,
Reich et al. 1990) that may be associated with mortality or
survival soon after fire. In one of the few studies on short-term
physiological responses of species to fire, Van Sambeek and
Pickard (1976a, 1976b) showed that scorching of leaves of
herbaceous species by fire was followed by rapid changes in
gas exchange of unheated leaves.
In an attempt to elucidate the mechanisms underlying the
physiological responses to fire of species that are differentially
tolerant of fire in natural ecosystems, we studied the effects on
gas exchange and survival of briefly heating surface roots and
stem bases of seedlings of red maple, sugar maple, white oak
(Quercus alba L.) and northern red oak (Quercus rubra L.).
Keywords: Acer saccharum, Acer rubrum, fire, photosynthesis,
Quercus alba, Quercus rubra, resprouting, survival, thermotolerance, transpiration.
Materials and methods
Introduction
In forest ecosystems, mortality caused by fire is selective
against many invading mesic species, suggesting that fire
might be used as a tool to control species composition and
diversity (Curtis 1959, Crow 1988). Fire is an important factor
in the establishment and maintenance of many oak-dominated
forests in the eastern USA, forests that otherwise would tend
to be replaced by more mesic, fire-sensitive species such as red
Seedling culture
Seeds of Q. alba, Q. rubra, A. rubrum, and A. saccharum were
collected from the Columbia area. Acorns and sugar maple
seed were collected in the fall of 1992, and red maple seed was
collected in the spring of 1991. Purchased red maple seed
(F.W. Schumacher Co., Inc., Sandwich, MA) was used in the
spring of 1993. Seeds were stratified and germinated according
to standard protocols (USDA Forest Service 1974).
Germinants were planted in a greenhouse in cylindrical
5.6-liter pots (15.3 cm diameter, 30.5 cm tall) filled with a
1/2/1 (v/v) mixture of peat moss, sand and silt loam. After
584
HUDDLE AND PALLARDY
planting, 30 ml of slow-release 14,14,14 N,P,K fertilizer (Osmocote, San Milpitas, CA) was placed on the soil surface and
30 ml of vermiculite layered on top to retard evaporation. Pots
were watered once a week, and fertilized weekly with modified Hoagland’s solution (Johnson et al. 1957). The temperature of the greenhouse ranged between 10 and 43 °C during the
study. Sunlight supplemented with sodium vapor lamps kept
midday irradiances at seedling tops at approximately 1000
µmol m −2 s −1 photosynthetic photon flux density (PPFD).
Growth chamber conditions and heating treatments
Before heat treatment, seedlings were moved from the greenhouse to a growth chamber and allowed to acclimate for at least
three days. The growth chamber provided a temperature of
25 °C and a 14-h photoperiod (400 µmol m −2 s −1 PPFD at the
top of the seedlings). Mean age at treatment ranged from 118
days for A. saccharum seedlings to 133 days for Q. alba
seedlings, with no significant differences among species (P ≤
0.05).
To simulate the heat of a passing ground fire, one of two
aluminum block heaters, one with a plate containing a 1.0 cm
slot and a 1.25 cm diameter hole, the other with a plate
containing a 2.0 cm slot and a 4.0 cm diameter hole, was used
(Figure 1). The block heater with the larger slot width and
central ring diameter was fabricated to reduce the number of
seedlings for which data had to be discarded because of inadvertent direct contact between the plate and stem. Two ceramic
cartridge heaters (Type 500B, Standard Electric Products Co.,
Dayton, OH) placed in holes drilled in the block provided
heating. Before the heat treatment was begun, the top of the
seedling was enclosed in a 2.54-liter water-cooled cuvette with
PPFD maintained at 2000 µmol m −2 s −1 with a multi-vapor
lamp (General Electric, Hendersonville, NC). Seedlings were
not removed from the cuvette until at least 60 min after applying heat.
After gas exchange had equilibrated, power (80 V, 7.5 amps)
was applied to the heaters and the heated block was then placed
on the soil. Mean duration of heat treatment ranged from 9.7
to 10.5 min with no significant differences among species.
Among species, mean maximum stem base temperature during
treatments ranged from 76.6 to 85.8 °C, with no significant
differences among species. Among individual seedlings, Tstem
ranged from 33 to 180 °C, and appeared to be dependent on
small differences in placement of the plate. Although there was
substantial variation in stem base temperature, it was not
unlike what might be expected in a natural surface fire event.
Nearly every heat treatment elicited a gas exchange response,
and variation in stem base temperature did not obscure species
differences in survival, resprouting or gas exchange responses.
Complete sets of gas exchange data were available for between
15 and 20 seedlings per species.
Temperatures at the base of the seedling stem and at three
soil depths in the pot were monitored throughout the gas
exchange measurements with copper-constantan thermocouples (Figure 2). Holes drilled on one side of the pot allowed
thermocouples to be inserted at several soil depths (Figure 1).
Leaf temperature and air temperature inside the cuvette were
also monitored.
Gas exchange measurements
Photosynthesis at 33--35 Pa ambient CO2 partial pressure and
transpiration were monitored with an open gas exchange system described by Ni and Pallardy (1991). Instrument outputs
were acquired every 10 s by a computerized data logger.
Photosynthesis (A, µmol m −2 s −1), transpiration (E, mmol m −2
s −1) and internal partial pressure of CO2 (Ci, Pa) were com-
Figure 1. Three-dimensional view of a heating plate and seedling.
Wires indicate the point at which two ceramic cartridge heaters were
inserted in the heating plate. Note sections of each pot were cut away
to facilitate placement of the heating plate and holes were drilled in the
side of each pot to provide for placement of thermocouples at several
soil depths. The top of the seedling was enclosed in a gas exchange
cuvette during the heating treatment.
Figure 2. Examples of temperatures during heating treatments. Symbols designate where temperatures were measured: (for Q. rubra 1) m
at stem base, h at 0.5 cm soil depth, , at 2.0 cm soil depth, n at
4.5 cm soil depth; (for A. saccharum 5) m at stem base, h at soil
surface, , at 1.5 cm soil depth, n at 4.0 cm soil depth.
STEM AND SOIL HEATING AND SEEDLING SURVIVAL
puted using equations of von Caemmerer and Farquhar (1981).
Photosynthesis and E of the heat-treated seedlings were monitored for several days after heating during which time seedlings were watered frequently. Because the pretreatment gas
exchange rates varied among seedlings, comparisons were
based on ratios of post-treatment to pretreatment values.
Water potential measurements
During the gas exchange measurements, the leaf water potential (Ψleaf ) of between six and eleven seedlings per species was
measured every 4 to 6 min with two leaf hygrometers (Model
L-51, Wescor, INC., Logan, UT) attached to leaves inside the
cuvette. The hygrometers were calibrated with KCl solutions
of known molality as described by Pallardy et al. (1991).
Assessment of survival and resprouting
Two weeks after heating, seedlings were moved from the
growth chamber back to the greenhouse. Watering and fertilization were conducted every week as described previously.
Resprouting and survival of all heat-treated seedlings (22--25
seedlings per species) were monitored for 12 weeks in the
greenhouse.
Statistical analysis
Chi-square tests were conducted to detect statistically significant differences among species in survival and resprouting
(Snedecor and Cochran, 1980). A chi-square test was also used
to detect statistically significant differences in survival between resprouting and non-resprouting seedlings.
Although soil temperatures increased in response to the heat
treatment, it was not possible to compare results across seedlings because of variations associated with measurement depth
and technical difficulties. Therefore, the maximum temperature measured at the base of the stem (Tstem ) was used as a
measure of temperature experienced by seedlings.
The statistical tests used to determine the significance of gas
exchange responses after heating were based on 95% tolerance
limits calculated for 1-min averages of gas exchange parameters (A, E, and Ci) measured before treatments were applied
(Hald, 1952). Similarly, the 95% tolerance limits of gas exchange responses 1 h after heat treatment were calculated from
585
1-min averages between 55 and 65 min after the heat treatment
was applied for each seedling. Responses 1 h after heating
were scored as 0, if the tolerance limits overlapped, or as 1 if
the tolerance limits did not overlap.
Short-term response scores (RS = 0 or 1) were then averaged
for each combination of species and three ranges of Tstem
(45--75, 75--105 and 105--135 °C). These averages were
arcsine transformed to normalize error as described by Box
and Cox (1964). The General Linear Models procedure of the
SAS version 6.08 software prgram (SAS Institute, Cary, NC)
was used to conduct analysis of variance (ANOVA) and to
calculate least square means with species and Tstem as treatment effects.
To analyze the magnitude of the short-term gas exchange
response, percent change in each parameter was calculated for
each seedling as follows:
%∆G s =
G 1 − G0
100 ,
G0
where %∆Gs is the short-term percent change in a gas exchange parameter, G1 is the mean of the parameter 1 h after
treatment and G0 is the mean of the parameter before heat was
applied. Percent changes in gas exchange were then arcsine
transformed to normalize error and analyzed by ANOVA with
species, response score 1 h after treatment (RS1 h) and the
interaction between species and response score as treatment
effects. Calculated least square means were subjected to the
t-test to determine whether they were significantly different
from zero.
Long-term changes in gas exchange parameters (%∆Gl)
were calculated and analyzed as describd for the short-term
changes. Data were pooled in two categories (1--2 days after
treatment, Dj = 1; and 6--8 days after treatment, Dj = 7) and
compared with pretreatment values:
%∆G 1 =
G j − G0
100 ,
G0
where Gj is the mean of the gas exchange parameter on day j
(Dj) after treatment and G0 is the mean of the gas exchange
Table 1. Survival and resprouting frequency of each species. Percentages in a row with different letters are significantly different (P ≤ 0.05).
Non-surviving seedlings
Non-resprouting
Resprouting
Total
Surviving seedlings
Non-resprouting
Resprouting
Total
% Survival
% Resprouting
Acer
rubrum
Acer
saccharum
Quercus
alba
18
0
18
21
0
21
10
3
13
2
1
3
51
4
55
1
3
4
1
0
1
1
11
12
4
18
19
7
32
39
4.5 c
0.0 b
48.0 b
56.0 a
88.0 a
76.0 a
41.5
38.3
18.2 c
13.6 b
Quercus
rubra
Total
586
HUDDLE AND PALLARDY
parameter before treatment. These percentages were transformed and analyzed by ANOVA with species, Dj and the
interaction between species and Dj as treatment effects. Each
least square mean was tested to detect whether it was significantly different from zero and back transformed to a percentage.
Results
Survival and resprouting
Survival among resprouting seedlings was significantly
greater (P ≤ 0.05) than among non-resprouting seedlings (88.9
versus 12.1%). Both Quercus species had significantly greater
survival and resprouting rates than either Acer species (Table 1), although only the difference in survival was statistically
significant. For all species, mean Tstem did not differ (P ≤ 0.05)
between non-surviving, non-resprouting seedlings (82.4 °C)
and surviving, resprouting seedlings (87.7 °C).
heat treatment than Acer seedlings. For all species, the shortterm percent change in photosynthetic rate, %∆As, declined
significantly only for seedlings with an RS = 1 (Table 3). Of
seedlings with an RS = 1, the relative reduction in A of
A. rubrum seedlings was significantly less than that of either
of the Quercus species. Internal CO2 partial pressure usually
increased, at least transiently, after heat application, except in
a few A. rubrum seedlings. For all seedlings, average %∆Ci,s
1 h after heat treatment was 1.4%. Mean %∆Ci,s increased for
all combinations of species and response scores after heat
treatment (Table 3).
Because the standard error of E increased between the pre-
Short-term gas exchange dynamics
At least 60% of all seedlings showed significant short-term
responses (i.e., RS = 1) in Ci, E and A to the heat treatment
(Table 2). Although the fraction of seedlings showing significant changes in Ci and E following heating increased with
increasing Tstem , the trend was not significant (P ≤ 0.15). In
contrast, the fraction of seedlings showing significant change
in A following heat treatment increased significantly (P ≤ 0.01)
with increasing Tstem (Table 2).
Heat-induced declines in A and E were usually apparent
within 1 h of heat treatment (cf. Figures 3 and 4). Averaged
across all species, seedlings showed a mean decline of 23.7%
in A 1 h after the heat treatment. Gas exchange of seedlings of
both Quercus species generally showed a greater response to
Table 2. Mean percent of seedlings showing significant responses (i.e.,
a response score of 1) in Ci, E and A by species and Tstem . Means by
species within a column with different lower case letters are significantly different (P ≤ 0.05); means by Tstem within a column with
different upper case letters are significantly different (P ≤ 0.05). All
means differed significantly from zero (P ≤ 0.05). P-values of models
used to calculate means given on the right.
Species
Acer rubrum
Acer saccharum
Quercus alba
Quercus rubra
Ci
E
A
67.4 a
61.2 a
86.3 a
64.2 a
78.7 ab
64.2 b
95.8 a
64.2 b
83.7 ab
72.3 b
95.3 a
82.1 ab
56.7 A
73.0 A
89.5 A
62.2 A
86.6 A
82.0 A
45.2 C
86.6 B
100.0 A
0.20
0.15
0.06
0.12
0.12
Q. alba
> A. rubrum ≈ A. saccharum. Seedlings of both Quercus
588
HUDDLE AND PALLARDY
Table 4. Mean long-term percent changes in Ci, E, and A from pretreatment values between one and two days after treatment (D1) and between six
and eight days after treatment (D7). For each species, means with different lower case letters are significantly different (P ≤ 0.05); for each day,
means with different upper case letters are significantly different (P ≤ 0.05). Means significantly different from zero (P ≤ 0.05) are designated with
asterisks.
Parameter
Day
A. rubrum
A. saccharum
%∆Ci,l
D1
D7
19.5 *a
9.6 *c
1.2 *f
4.5 *e
%∆El
D1
D7
17.7 *a
−32.7 *d
−4.5 b
−18.0 *c
%∆Al
D1
D7
23.7 *a
−34.3 *c
8.9 *b
8.9 *b
species showed significantly greater resprouting rates after
heating than did seedlings of either Acer species, suggesting
that the capacity of Quercus species to resprout after exposure
to lethal stem temperatures enables them to survive fire better
than Acer species (Huddle 1995).
Decreases in E and A and slight increases in Ci were observed after soil and stem base heating was applied, indicating
that changes in leaf gas exchange can occur in response to
application of heat to tissues remote from the leaf (Sinyukhin
and Gorchakov 1966, Van Sambeek and Pickard 1976b). Hydraulic signals may induce physiological responses in tissues
not directly exposed to a variety of stresses, including heat
(Malone 1993, Malone et al. 1994). One type of hydraulic
signal that might be associated with thermal responses is a
change in Ψ. If a hydraulic pulse associated with heating
lowered Ψ of cells surrounding guard cells, the latter may lose
water through passive water movement, resulting in stomatal
closure (Malone 1993). Changes in Ψleaf observed in the present study do not support this hypothesis. The decreases in
water potential never exceeded −0.5 MPa and were usually
smaller, and Ψleaf values never declined to the range over which
stomatal closure might be expected (Bahari et al. 1985, Ni and
Pallardy 1991, 1992). Because Ψleaf remained relatively high
after heating and did not drop more rapidly than E or A, we
conclude that changes in Ψ were not associated with the
heat-induced reductions in A.
An alternative hypothesis is that the declines in E following
heat application are the result of a series of events triggered by
propagation of action potentials that changes guard cell turgor
and causes stomatal closure (Davies 1987, Davies et al. 1991).
Studies with herbaceous plants have shown that if a stimulus
such as heat, cutting or a series of electrical pulses is sufficient
to cause a measurable action potential, a change in gas exchange follows (Gunar and Sinyukhin 1963, Sinyukhin and
Gorchakov 1968, Van Sambeek and Pickard 1976b, Dziubiñska et al. 1989).
Besides lowering E, heat treatment reduced A. Because
stomatal closure reduces availability of CO2, Ci should decline
if stomatal closure is largely responsible for reduced A. However, Ci of most seedlings increased after heat treatment, sug-
Q. alba
Q. rubra
3.2* ef
13.4* b
5.0 *e
7.4 *d
7.2 *B
8.7 *A
−18.6* c
−0.8* c
−32.2 *d
−23.2 *c
−9.4 *A
−18.7 *B
−35.3* c
−60.6* e
−48.9 *d
−56.4 *de
−12.9 *A
−35.6 *B
All species
gesting that increased mesophyll resistance was at least partly
responsible for the observed reductions in A.
On the days following heat treatment, seedlings of both
Quercus species underwent a progressive and more substantial
loss in photosynthetic capacity than seedlings of the Acer
species, whereas we had expected that species more capable of
surviving fire (i.e., Quercus) would maintain or regain physiological function more fully after heating than more poorly
adapted species such as Acer. We postulate that the inverse
relationship between photosynthetic capacity and survival following heat treatment is related to the plant’s capacity to
resprout. Our results indicate that the resprouting response,
which was more vigorous in Quercus species than in Acer
species, is an alternate and effective, but resource-intensive,
adaptation to fire. Based on our results and the findings of other
studies, we suggest that Quercus spp. respond to heat injury
by: (1) abandoning heat-injured shoots; (2) promoting rapid
compartmentalization of injured from healthy tissues by the
production of a suberin layer (McDougall 1993); (3) promoting release from hormonal inhibition associated with apical
dominance of living stems (Vogt and Cox, 1970); and (4)
promoting reallocation of resources to the resprouting response.
Physiological and shoot mortality responses to even moderate heating were substantial, and thus many surface fires in
natural forests could be expected to elicit similar responses in
small individuals to those observed in this study. The more
vigorous resprouting capacity of Quercus compared to Acer
seedlings appears to be a key feature of the successful adaptation of Quercus species to fire. This difference could be exploited to promote greater relative abundance of Quercus
regeneration in deciduous forests of eastern North America.
Acknowledgments
Research was supported by the McIntire-Stennis Program. The
authors thank N. Loewenstein and J. Rhoads for greenhouse assistance, John Roberts for technical assistance, and Dr. G. Krause for
suggestions on statistical analysis.
STEM AND SOIL HEATING AND SEEDLING SURVIVAL
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